Metabolic preference of nitrate over oxygen as an electron acceptor in foraminifera from the Peruvian oxygen minimum zone

Nicolaas Glock, Alexandra-Sophie Roy, Dennis Romero, Tanita Wein, Julia Weissenbach, Niels Peter Revsbech, Signe Høgslund, David Clemens, Stefan Sommer, and Tal Dagan
PNAS February 19, 2019 116 (8) 2860-2865; first published February 19, 2019 https://doi.org/10.1073/pnas.1813887116

  1. Edited by David M. Karl, University of Hawaii, Honolulu, HI, and approved January 4, 2019 (received for review August 11, 2018)

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Significance

Foraminifera are able to respire nitrate instead of oxygen, a rare ability amongst eukaryotes. Here, we show that benthic foraminifera from the Peruvian oxygen minimum zone are not just facultative anaerobes by switching to nitrate respiration when oxygen is depleted but that denitrification is their preferred respiration pathway. Their metabolic adaptations allow some species to grow larger than predicted by cell physiology of aerobic organisms due to oxygen limitation. Finally, we formulate, from our observations, mathematical equations to predict the amount of foraminiferal denitrification using their cell volume. Nitrate is an important macronutrient, and denitrification is the main oceanic nitrate sink. Our equations will help to constrain biogeochemical models for marine nitrate cycling.

Abstract

Benthic foraminifera populate a diverse range of marine habitats. Their ability to use alternative electron acceptors—nitrate (NO3−) or oxygen (O2)—makes them important mediators of benthic nitrogen cycling. Nevertheless, the metabolic scaling of the two alternative respiration pathways and the environmental determinants of foraminiferal denitrification rates are yet unknown. We measured denitrification and O2 respiration rates for 10 benthic foraminifer species sampled in the Peruvian oxygen minimum zone (OMZ). Denitrification and O2 respiration rates significantly scale sublinearly with the cell volume. The scaling is lower for O2 respiration than for denitrification, indicating that NO3− metabolism during denitrification is more efficient than O2 metabolism during aerobic respiration in foraminifera from the Peruvian OMZ. The negative correlation of the O2 respiration rate with the surface/volume ratio is steeper than for the denitrification rate. This is likely explained by the presence of an intracellular NO3− storage in denitrifying foraminifera. Furthermore, we observe an increasing mean cell volume of the Peruvian foraminifera, under higher NO3− availability. This suggests that the cell size of denitrifying foraminifera is not limited by O2 but rather by NO3− availability. Based on our findings, we develop a mathematical formulation of foraminiferal cell volume as a predictor of respiration and denitrification rates, which can further constrain foraminiferal biogeochemical cycling in biogeochemical models. Our findings show that NO3− is the preferred electron acceptor in foraminifera from the OMZ, where the foraminiferal contribution to denitrification is governed by the ratio between NO3− and O2.

Footnotes

  • ↵1To whom correspondence should be addressed. Email: nglock{at}geomar.de.

  • ↵2Present address: Faculty of Biology, Technion–Israel Institute of Technology, 320000 Haifa, Israel.

  • Author contributions: N.G., A.-S.R., N.P.R., S.H., and T.D. designed research; N.G., A.-S.R., D.R., T.W., J.W., D.C., S.S., and T.D. performed research; N.P.R. contributed new reagents/analytic tools; N.G., D.C., and S.S. analyzed data; and N.G. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1813887116/-/DCSupplemental.

Published under the PNAS license.

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Metabolic preference of nitrate over oxygen as an electron acceptor in foraminifera from the Peruvian oxygen minimum zone
Nicolaas Glock, Alexandra-Sophie Roy, Dennis Romero, Tanita Wein, Julia Weissenbach, Niels Peter Revsbech, Signe Høgslund, David Clemens, Stefan Sommer, Tal Dagan
Proceedings of the National Academy of Sciences Feb 2019, 116 (8) 2860-2865; DOI: 10.1073/pnas.1813887116
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